Heterologous expression of family 10 xylanases from Acidothermus cellulolyticus enhances the exoproteome of Caldicellulosiruptor bescii and growth on xylan substrates

Kim, Sun -Ki; Chung, Daehwan; Himmel, Michael E.; Bomble, Yannick J.; Westpheling, Janet

doi:10.1186/s13068-016-0588-9

Title: Heterologous expression of family 10 xylanases from Acidothermus cellulolyticus enhances the exoproteome of Caldicellulosiruptor bescii and growth on xylan substrates

Abstract

The ability to deconstruct plant biomass without conventional pretreatment has made members of the genus Caldicellulosiruptor the target of investigation for the consolidated processing of lignocellulosic biomass to biofuels and bioproducts. These Gram-positive bacteria are hyperthermophilic anaerobes and the most thermophilic cellulolytic organisms so far described. They use both C5 and C6 sugars simultaneously and have the ability to grow well on xylan, a major component of plant cell walls. This is an important advantage for their use to efficiently convert biomass at yields sufficient for an industrial process. For commodity chemicals, yield from substrate is perhaps the most important economic factor. In an attempt to improve even further the ability of C. bescii to use xylan, we introduced two xylanases from Acidothermus cellulolyticus. Acel_0180 includes tandem carbohydrate-binding modules (CBM2 and CBM3) located at the C-terminus, one of which, CBM2, is not present in C. bescii. Also, the sequences of Xyn10A and Acel_0180 have very little homology with the GH10 domains present in C. bescii. For these reasons, we selected these xylanases as potential candidates for synergistic interaction with those in the C. bescii exoproteome. As a result, heterologous expression of two xylanases from Acidothermus cellulolyticus in Caldicellulosiruptor bescii resultedmore »« less

Authors:

Kim, Sun -Ki ^[1]; Chung, Daehwan ^[2]; Himmel, Michael E. ^[2]; Bomble, Yannick J. ^[2]; Westpheling, Janet ^[1]

Univ. of Georgia, Athens, GA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
National Renewable Energy Lab. (NREL), Golden, CO (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Publication Date:: Mon Aug 22 00:00:00 EDT 2016

Research Org.:: National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1319281

Report Number(s):: NREL/JA-2700-67046
Journal ID: ISSN 1754-6834

Grant/Contract Number:: AC36-08GO28308; AC05-00OR22725

Resource Type:: Accepted Manuscript

Journal Name:: Biotechnology for Biofuels

Additional Journal Information:: Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 1754-6834

Publisher:: BioMed Central

Country of Publication:: United States

Language:: English

Subject:: 09 BIOMASS FUELS; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; consolidated bioprocessing; biomass deconstruction; xylanase; caldicellulosiruptor

Citation Formats


                    Kim, Sun -Ki, Chung, Daehwan, Himmel, Michael E., Bomble, Yannick J., and Westpheling, Janet. Heterologous expression of family 10 xylanases from Acidothermus cellulolyticus enhances the exoproteome of Caldicellulosiruptor bescii and growth on xylan substrates.  United States: N. p., 2016. 
Web.  doi:10.1186/s13068-016-0588-9.

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                    Kim, Sun -Ki, Chung, Daehwan, Himmel, Michael E., Bomble, Yannick J., & Westpheling, Janet. Heterologous expression of family 10 xylanases from Acidothermus cellulolyticus enhances the exoproteome of Caldicellulosiruptor bescii and growth on xylan substrates.  United States.  https://doi.org/10.1186/s13068-016-0588-9

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                    Kim, Sun -Ki, Chung, Daehwan, Himmel, Michael E., Bomble, Yannick J., and Westpheling, Janet. Mon .  
"Heterologous expression of family 10 xylanases from Acidothermus cellulolyticus enhances the exoproteome of Caldicellulosiruptor bescii and growth on xylan substrates".  United States.  https://doi.org/10.1186/s13068-016-0588-9.  https://www.osti.gov/servlets/purl/1319281.

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@article{osti_1319281,

  title        = {Heterologous expression of family 10 xylanases from Acidothermus cellulolyticus enhances the exoproteome of Caldicellulosiruptor bescii and growth on xylan substrates},

  author       = {Kim, Sun -Ki and Chung, Daehwan and Himmel, Michael E. and Bomble, Yannick J. and Westpheling, Janet},

  abstractNote = {The ability to deconstruct plant biomass without conventional pretreatment has made members of the genus Caldicellulosiruptor the target of investigation for the consolidated processing of lignocellulosic biomass to biofuels and bioproducts. These Gram-positive bacteria are hyperthermophilic anaerobes and the most thermophilic cellulolytic organisms so far described. They use both C5 and C6 sugars simultaneously and have the ability to grow well on xylan, a major component of plant cell walls. This is an important advantage for their use to efficiently convert biomass at yields sufficient for an industrial process. For commodity chemicals, yield from substrate is perhaps the most important economic factor. In an attempt to improve even further the ability of C. bescii to use xylan, we introduced two xylanases from Acidothermus cellulolyticus. Acel_0180 includes tandem carbohydrate-binding modules (CBM2 and CBM3) located at the C-terminus, one of which, CBM2, is not present in C. bescii. Also, the sequences of Xyn10A and Acel_0180 have very little homology with the GH10 domains present in C. bescii. For these reasons, we selected these xylanases as potential candidates for synergistic interaction with those in the C. bescii exoproteome. As a result, heterologous expression of two xylanases from Acidothermus cellulolyticus in Caldicellulosiruptor bescii resulted in a modest, but significant increase in the activity of the exoproteome of C. bescii on xylan substrates. Even though the increase in extracellular activity was modest, the ability of C. bescii to grow on these substrates was dramatically improved suggesting that the xylan substrate/microbe interaction substantially increased deconstruction over the secreted free enzymes alone. In conclusion, we anticipate that the ability to efficiently use xylan, a major component of plant cell walls for conversion of plant biomass to products of interest, will allow the conversion of renewable, sustainable, and inexpensive plant feedstocks to products at high yields.},

  doi          = {10.1186/s13068-016-0588-9},

  journal      = {Biotechnology for Biofuels},

  number       = 1,

  volume       = 9,

  place        = {United States},

  year         = {Mon Aug 22 00:00:00 EDT 2016},

  month        = {Mon Aug 22 00:00:00 EDT 2016}

}

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https://doi.org/10.1186/s13068-016-0588-9

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Figures / Tables:

Table 1: List of glycoside hydrolase Family 10 (GH10) catalytic domains in Caldicellulosiruptor bescii and their sequence homology with the GH10 domains in Acel_0180 and Acel_0372 xylanases from A. cellulolyticus

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Works referencing / citing this record:

Genomic and physiological analyses reveal that extremely thermophilic Caldicellulosiruptor changbaiensis deploys uncommon cellulose attachment mechanisms
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Khan, Asma M. A. M.; Mendoza, Carl; Hauk, Valerie J.
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Genome Stability in Engineered Strains of the Extremely Thermophilic Lignocellulose-Degrading Bacterium Caldicellulosiruptor bescii
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Williams-Rhaesa, Amanda M.; Poole, Farris L.; Dinsmore, Jessica T.
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In vivo synergistic activity of a CAZyme cassette from Acidothermus cellulolyticus significantly improves the cellulolytic activity of the C. bescii exoproteome

Journal Article Kim, Sun -Ki ; Chung, Daehwan ; Himmel, Michael E. ; ... - Biotechnology and Bioengineering

The use of microbial cells to convert plant biomass directly to fuels and chemicals is referred to as consolidated bioprocessing (CBP). Members of the bacterial genus, Caldicellulosiruptor (Gram-positive, anaerobic hyperthermophiles) are capable of deconstructing plant biomass without enzymatic or chemical pretreatment. This is accomplished by the production and secretion of free, multi-domain enzymes that outperform commercial enzyme cocktails on some substrates. Here, we show that the exoproteome of C. bescii may be enhanced by the heterologous expression of enzymes from Acidothermus cellulolyticus that act synergistically to improve sugar release from complex substrates; as well as improve cell growth. In thismore »« less
Cited by 10
https://doi.org/10.1002/bit.26366

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Heterologous co-expression of two β-glucanases and a cellobiose phosphorylase resulted in a significant increase in the cellulolytic activity of the Caldicellulosiruptor bescii exoproteome

Journal Article Kim, Sun-Ki ; Chung, Daehwan ; Himmel, Michael E. ; ... - Journal of Industrial Microbiology and Biotechnology

The ability to deconstruct plant biomass without conventional pretreatment has made members of the genus Caldicellulosiruptor the target of investigation for the consolidated processing of plant lignocellulosic biomass to biofuels and bioproducts. To investigate the synergy of enzymes involved and to further improve the ability of C. bescii to degrade cellulose, we introduced CAZymes that act synergistically with the C. besciii exoproteome in vivo and in vitro. We recently demonstrated that the Acidothermus cellulolyticus E1 endo-1,4-β-D-glucanase (GH5) with a family 2 carbohydrate-binding module (CBM) increased the activity of C. bescii exoproteome on biomass, presumably acting in concert with CelA. Themore »« less
Cited by 8
https://doi.org/10.1007/s10295-019-02150-0
Characterization of the Biomass Degrading Enzyme GuxA from Acidothermus cellulolyticus

Journal Article Hengge, Neal N. ; Mallinson, Sam J. B. ; Pason, Patthra ; ... - International Journal of Molecular Sciences (Online)

Microbial conversion of biomass relies on a complex combination of enzyme systems promoting synergy to overcome biomass recalcitrance. Some thermophilic bacteria have been shown to exhibit particularly high levels of cellulolytic activity, making them of particular interest for biomass conversion. These bacteria use varying combinations of CAZymes that vary in complexity from a single catalytic domain to large multi-modular and multi-functional architectures to deconstruct biomass. Since the discovery of CelA from Caldicellulosiruptor bescii which was identified as one of the most active cellulase so far identified, the search for efficient multi-modular and multi-functional CAZymes has intensified. One of these candidates,more »« less
https://doi.org/10.3390/ijms23116070
Heterologous expression of a β- d -glucosidase in Caldicellulosiruptor bescii has a surprisingly modest effect on the activity of the exoproteome and growth on crystalline cellulose

Journal Article Kim, Sun-Ki ; Chung, Daehwan ; Himmel, Michael E. ; ... - Journal of Industrial Microbiology and Biotechnology

Members of the genus Caldicellulosiruptor are the most thermophilic cellulolytic bacteria so far described and are capable of efficiently utilizing complex lignocellulosic biomass without conventional pretreatment. Previous studies have shown that accumulation of high concentrations of cellobiose and, to a lesser extent, cellotriose, inhibits cellulase activity both in vivo and in vitro and high concentrations of cellobiose are present in C. bescii fermentations after 90 h of incubation. For some cellulolytic microorganisms, β-d-glucosidase is essential for the efficient utilization of cellobiose as a carbon source and is an essential enzyme in commercial preparations for efficient deconstruction of plant biomass. Inmore »« less
Cited by 5
https://doi.org/10.1007/s10295-017-1982-4

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MOESM1 of Heterologous expression of family 10 xylanases from Acidothermus cellulolyticus enhances the exoproteome of Caldicellulosiruptor bescii and growth on xylan substrates
text, January 2016

Kim, Sun-Ki; Chung, Daehwan; Himmel, Michael
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DOI: 10.6084/m9.figshare.c.3623930_d1
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